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,3,**
* DSM Food Specialties, R&D-FTD, 2600 MA Delft;
Animal Nutrition Group,
** Adaptation Physiology Group, and
Fish Culture and Fisheries Group, Wageningen University & Research Center, 6700 AH Wageningen, The Netherlands
3To whom correspondence should be addressed. E-mail: arie.kies{at}dsm.com.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • piglet • phytase • energy metabolism • mineral absorption • mineral excretion
Most of the phosphorus (P) in vegetable feedstuffs is in phytate. Phytate is degraded only to a limited extent in the gastrointestinal tract of monogastric animals, hampering the availability of P for these animals. This results in a high P excretion in feces, which may result in pollution of the environment in areas with intensive animal husbandry. The negatively charged phytate ions can form strong complexes with cationic minerals and other positively charged compounds in the gastrointestinal tract (1–6).
To improve the availability of P of vegetable origin in the diets of pigs and poultry, microbial phytase is widely used as a feed additive. Phytase hydrolyzes phosphate groups from phytate, and increases the availability of P. An additional advantage is that phytase may also improve feed efficiency, as was calculated from experiments performed with piglets fed diets not limiting in digestible P (7). This effect, which may be as high as 3%, has several possible explanations. First, phosphorus availability may be increased. The P requirement assumed does not necessarily give maximum performance. However, a digestible phosphorus level slightly above the requirement has little effect on performance (8). Second, the solubility of cationic minerals (e.g., Ca, Zn, and Fe) and proteins that are complexed to phytate may be increased. These nutrients are released when phytase hydrolyzes phosphate groups from phytate (3,9–13). Because (micro-) minerals, except Ca, P, and Na, are usually added to feeds in excess of the requirement of animals, it is unlikely that their improved bioavailability enhances animal performance. Amino acid digestibility may be increased by phytase supplementation (7). It was calculated (14) that this could explain only 10–25% of the performance effects. The improvement of amino acid digestibility, however, is often small and not significant (15). Third, energy utilization may be increased, e.g., due to greater digestion of starch or fat (16,17). In several studies, however, no positive effect of phytase addition on energy digestibility was observed (18,19).
In the earlier studies, the effect of phytase on postabsorptive energy metabolism and protein gain was not investigated. We hypothesized that phytase may improve performance by a change in energy metabolism. More specifically: 1) Less energy is excreted with urine and feces as a result of increased digestion (e.g., of fat and starch), or of reduced excretion of endogenous protein (20). 2) Maintenance energy is reduced. Energy expenditure may be lower for nutrient transport (21) or for gastrointestinal tissues and absorptive processes. Phytate can bind digestive enzymes, which could result in an increased need for enzyme production via a negative feedback mechanism (13,22). Phytate degradation would result in the production of a smaller amount of digestive enzymes. 3) Increased mineral absorption may cost energy to the piglet. Minerals absorbed in excess of their requirement will be largely excreted via urine. Absorption and excretion are both (partly) ATP-requiring processes and can, therefore, affect energy metabolism (21,23,24). A difference in energy metabolism may result in performance differences, or in an alteration of the composition of retained energy. A shift in available energy or protein may change the rates of protein and fat deposition (25).
The objective of the present experiment was to investigate whether dietary microbial phytase supplementation affects utilization and partitioning of energy in young piglets. Increased absorption and excretion of ash, Ca, P, Na, K, Mg, Cu, Fe, and Cl were quantified, and the energy costs required for these processes were estimated using a mathematical model.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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46 d of age (11.3 ± 0.25 kg), which was 3 wk after weaning. The ethical committee of Wageningen University and Research Center approved the experiment described. At the start of the experiment, piglets were assigned to 1 of 2 dietary treatments (control vs. phytase supplementation) based on weight and litter. Each group of 8 piglets was housed in 1 of 2 identical climate respiration chambers (2.5 x 1.5 m), comparable in design to those described previously (26). Ambient temperature was maintained at 25, 24, and 23°C during wk 1, 2, and 3, respectively. Relative humidity was maintained at 65% (range 60–70%). Air velocity was <0.20 m/s. A 12-h light:dark cycle was used.
At the start of the experiment, piglets were switched immediately to the experimental diets, offered at 2.3 times energy requirements for maintenance (MEm).4 The 2 diets were identical in composition (Table 1), except for the addition of phytase [1500 phytase units (FTU)/kg feed; Natuphos®] to one of the diets. It was shown (28,29) that the maximal effect of phytase on P digestibility is reached at 1000–1500 FTU/kg. To study the direct effect of phytase on energy metabolism, diets were formulated to be limiting in energy, i.e., the ileal digestible lysine/digestible energy (DE) ratio was 0.74. This is 10% higher than the recommended dietary level of lysine in relation to energy content for piglets of 10–20 kg body weight (30,31). Diets were not limiting in other nutrients (31,32), and were adequate in digestible P (33). Both diets were high in phytate P (3.8 g/kg) to ensure substrate availability. Because feeding Ca and P slightly above requirement does not affect performance (8), we assumed that the Ca and P released by phytase would not affect energy metabolism. Mineral levels (Table 1) ranged between the value recommended by the NRC (32) for Na and 8 times the recommendation for Fe. The Cu level was far in excess of the requirement of 5 mg/kg feed, as is common in practice. Diets were pelleted at a temperature < 70°C to prevent loss of enzyme activity. Piglets had free access to water. On the day of slaughter, piglets consumed their respective diets ad libitum for 4 h before slaughter.
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Total heat production (Htot) was measured in 9-min intervals by measuring the exchange of oxygen, carbon dioxide, and methane (26) using Brouwer’s formula (34). Htot was measured during the last 5, 6, and 6 d of the 3 periods, respectively. The respiration chamber had to be opened twice daily to feed the piglets. Heat measurements are, therefore, based on 22 h/d. Energy retention was calculated by subtracting Htot from ME intake. MEm was estimated based on Agricultural Research Council data (35), assuming efficiencies of 54% for protein, and 74% for fat retention.
Physical activity was recorded in the same time intervals as Htot. Physical activity per group of piglets was monitored with a radar device according to the method of Wenk and Van Es (36). Calculations of activity-related heat production (Hact) and heat production corrected for activity (Hrest) were done as described by Gentry et al. (37).
Apparent fecal digestibility and urinary mineral excretion. For measurement of apparent fecal digestibility, fresh "grab" samples were taken daily from each group of pigs directly after the morning feeding, taking care to collect feces from different piglets. These samples were taken for 5, 6, and 6 d in periods 1–3. The feces (100 g/d) were pooled each period and stored at –20°C before analyses. Apparent fecal digestibilities were calculated using acid-insoluble ash as a marker (38). Mineral excretion in urine was calculated from the difference of the quantities excreted with feces + urine and feces alone.
Measurements at slaughter. One day after the last balance period, the pigs consumed their feed ad libitum for 4 h. Then they were weighed, anesthetized, and the abdominal cavity was opened and directly 2 blood samples were taken from the portal vein. Within 3 min, 1 sample was analyzed for pH, partial oxygen pressure (pO2) and partial carbon dioxide pressure (pCO2) using i-STAT cartridges. The other blood sample was collected into a heparinized tube (Li-Heparin) and stored on ice. Within 4 h, this sample was centrifuged at 1100 x g for 12 min, and plasma was stored at –20°C for analysis of mineral contents. After the blood samples were taken, pigs were killed by injection of 1 mL of T61 directly into the portal vein. Weights of the emptied gastrointestinal tract (separated in stomach, small intestine, cecum and colon + rectum), pancreas, liver, kidneys (without fat), and heart were recorded.
Analytical procedures. Kjeldahl nitrogen was analyzed (39) in feed, feces (fresh), mixed feces + urine (fresh), in condensated water collected from the respiration chambers, and in acidified liquid samples through which outflowing air from the chambers was led to trap gaseous ammonia. Crude fat, crude ash, acid-insoluble ash, and energy were analyzed in feed, freeze-dried feces, and freeze-dried feces + urine. Crude fat was analyzed after acid hydrolysis by extraction with petroleum ether [boiling range 40–60°C; (40)]. Crude ash and acid-insoluble ash were analyzed according to International Organization for Standardization methods (41,42). Energy content was analyzed using adiabatic bomb calorimetry (IKA-C700, Janke & Kunkel). Feed samples were analyzed for phytic acid (43) and phytase activity (44).
Minerals and chloride were determined in feed and freeze-dried samples of feces and feces + urine. Minerals were measured by inductively coupled plasma atomic emission spectrometry (ICP-AES) using yttrium as an internal standard (45). Chloride was measured titrimetrically after water extraction from the samples (46). Heparinized blood plasma samples were analyzed electrochemically for Na, K, Cl, Ca (ionized), lactate, and glucose, using an EML 105 (Radiometer). Blood P was determined in plasma samples after deproteinization with trichloroacetic acid by ICP-AES.
Model calculations. Potential energy costs associated with the increased absorption of amino acids, fatty acids, and minerals from the gastrointestinal tract, increased retention of Ca and P in bone tissues, and increased tubular reabsorption of minerals from primary urine due to phytase supplementation were estimated using a model. A complete model description is provided in Appendix 1 (available online at www.nutrition.org). Calculations were performed using Excel® 2000 (Microsoft). The "Goal Seek" tool of Excel was used to calibrate renal reabsorption of the different minerals to the mineral excretion rates, observed in present experiment.
Statistical analyses.
For all traits, group was the experimental unit. Data for GE, ME, ER, ERp, ERf, Htot, Hact, and Hrest were expressed in kJ/(kg0.75 · d). The effect of phytase supplementation was tested with the GLM procedure of SAS (Version 6.12; SAS Institute) by means of F-tests using a split-plot model, with balance period values within groups taken as repeated measurements:
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where Yijkl = trait; µ = overall mean; Ti = fixed effect of subtrial i (i = 1, ..., 4); Fj = fixed effect of experimental diet j (j = control, phytase); e1,ijk = error term 1, which represents the random effect of group k (k = 1, ..., 4) nested within trial i and feeding treatment j; Wl = fixed effect of balance period l (l = 1, 2, 3); e2,ijkl = error term 2. The effects of trial and experimental diet were tested against error term 1, other effects against error term 2. Results are presented as Least Square Means with their SE. The number of observations per treatment per trait was thus 12.
For traits measured at the end of each subtrial at slaughter (blood variables and weights of organs and intestines), the model was used without period effect:
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with 4 observations per treatment per trait.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Weight gain of piglets was slightly higher in those administered phytase than for control piglets (329 vs. 319 ± 4 g/d). Because feed intakes did not differ (484 g/d), the gain:feed ratio tended to be greater in the phytase group (681 vs. 661 ± 7 g/kg, P = 0.13).
Digestibility.
Phytase tended (P 
0.10) to increase apparent fecal digestibility of dry matter, nitrogen, fat, and energy by 2.0, 1.9, 1.2, and 1.3%, respectively (Table 2). Phytase increased ash digestibility by almost 10% (P < 0.05). For all nutrients, apparent fecal digestibility increased with time (P < 0.01). There was no week x feed interaction, except for ash (P < 0.01). Ash digestibility was higher in pigs fed phytase than in those fed the control diet, but the difference became smaller over time.
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In portal blood of piglets fed phytase (4 h after ad libitum consumption of feed), the pH was lower (P < 0.01), and partial carbon dioxide pressure was higher (P < 0.01; Table 4). Plasma glucose, K, and P concentrations were 20% (P < 0.05), 31% (P < 0.01), and 18% (P < 0.07) higher, respectively, in phytase-fed piglets than in control piglets. Plasma concentrations of Na, Cl and Ca were unaffected by treatment.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Effect of phytase on energy utilization. Apparent fecal digestibility of energy was higher in phytase-supplemented piglets, which could be attributed mainly to higher protein and fat digestibilities. The positive effect of dietary phytase on fecal protein digestibility was reported previously (18,47), but the magnitude of the effect was often small (19,48). The effect of phytase on fecal fat digestibility was measured in a few experiments, mainly with a positive effect (49). In general, no improvement of energy digestibility was reported (18,19,48).
Energy metabolizability did not differ for the 2 treatments (82.7 vs. 82.5% for phytase and control, respectively). Consequently, energy losses in urine and gases were higher in phytase-supplemented piglets (13 and 1.2 kJ/(kg0.75 · d), respectively; Table 3). Diets were designed to be limiting in energy. It could, therefore, be expected that more nitrogenous components would be excreted in the urine of piglets administered phytase, given the higher protein digestibility (Table 2). Piglets excreted 0.67 (phytase) or 0.64 (control) g N/(kg0.75 · d) in urine, which explains only 1 kJ/(kg0.75 · d) of the difference in urinary energy. The remaining difference, 12 kJ/(kg0.75 · d) (1.3% of ME intake) cannot be attributed to urinary loss of nitrogenous compounds. Explaining this gap requires more extensive urinary measurements that were not performed in present experiment. We speculate that because dietary phytase increased the mineral absorption rate (discussed later), this could increase blood plasma volume, and consequently blood pressure. As a result, more plasma compounds would be filtered into the primary urine, and have to be reabsorbed. Possibly, with the increase in renal ultra filtration, more (energy-rich) organic compounds that are normally reabsorbed are lost in urine. For instance, reabsorption of glucose is almost, but not totally complete (50). Increased renal filtration may increase urinary losses of glucose, or similar energy-rich compounds. This requires further investigation.
In fast-growing poultry, dietary phytase clearly enhances energy metabolizability. A mean increase of ME content with 220 kJ/kg feed was calculated, when 500 FTU/kg feed was supplied (7). This is 1.8% of the ME content of a typical broiler diet. In the present experiment, phytase supplementation increased the ME content of the diet for piglets by only 0.3%.
No difference in energy partitioning was observed between treatments. In a preliminary, unpublished, experiment with newly weaned piglets consuming feed ad libitum, there were indications that retention might be increased with phytase supplementation. Energy retention increased by 17%, but this was largely the result of a higher feed intake. In an experiment with growing pigs (26–52 kg) fed restricted diets (2.9 x MEm), phytase supplementation to diets not limiting in P increased energy retention by 6% compared with control pigs, as measured by total-body electrical conductivity on carcasses (51). In both experiments, the effects were not significant, however.
Organ weight and blood variables. After the experimental period of 21 d, weights of the pancreas and small intestine were slightly lower in phytase than in control piglets. Lower pancreas weight might be due to a lower production of pancreatic digestive enzymes because a smaller amount of these enzymes are bound to phytate (13,20,22). The reduction in small intestine weight was not significant. These findings may indicate that work required for digestive processes is slightly less (30,52,53). Corresponding to the increased digestibility, it could mean that the digestion process is facilitated by phytase.
One sample of portal blood was taken from each piglet 4 h after the initiation of feeding. Because kinetic information is lacking, no firm conclusions on metabolic activity in visceral tissues can be drawn. Some interesting differences occurred between treatments, however. The pH, typically 7.4 (54), was very low in both treatment groups, i.e., 7. Lower pH and pO2, and higher pCO2 were observed in phytase-treated piglets. This could indicate increased oxidative metabolism in portal-drained viscera at the time of sampling, due to a higher absorption rate of nutrients. Increased metabolic activity of the viscera was not reflected, however, in higher heat production at 4 h postfeeding (data not shown). Higher absorption of Na and K coincides with increased bicarbonate absorption, which may also explain the higher pCO2 of portal blood (54). Absorption of sodium requires oxygen, due to the activity of Na, K-ATPase (21,23), which could explain the slightly lower pO2.
Portal plasma glucose concentration was 21% higher in phytase-treated piglets than in control piglets. Blood glucose level depends on many factors, including insulin, which we did not measure. It may reflect a higher rate of absorption from the viscera, a lower utilization by visceral tissues, a lower portal blood flow, or a combination of these factors. A higher absorption rate would agree with the higher energy digestibility. For both treatments, starch digestibility was almost complete at the end of the ileum (data not shown); thus the extent of starch digestion cannot explain the higher plasma glucose concentration. The findings for glucose agree with those of Johnston et al. (48), who found a higher plasma glucose level (5%) in pigs administered phytase. They took a blood sample from the vena cava, which is an important difference from our experiment (portal vein). In the current experiment, we compared pH, pO2, and pCO2 in portal and in jugular blood of 6 piglets. The mean values (phytase and control) for these 3 variables were 7.07, 5.0, and 11.5 for portal blood, and 7.27, 5.6, and 6.6 for jugular blood, respectively. These values are not indicative of glucose concentration, but indicate that caution is required when comparing results of blood sampled from different veins.
Together, these blood variables suggest that gut metabolism is more intensive in phytase-treated piglets 4 h after the start of feeding. But this did not result in changes in heat production. Dietary phytase may simultaneously both increase and decrease heat production, resulting in no net effect. A higher mineral load might increase heat production. First, minerals are absorbed; when they are absorbed in excess of the piglet’s needs, they must be excreted. Both absorption and excretion are partially active processes, thus requiring energy.
Effect of phytase on mineral metabolism. Dietary phytase supplementation increased apparent fecal ash digestibility by almost 10%. This is the result of increased absorption of all minerals studied and is in agreement with earlier findings (11,55–58). In those studies, the effect of phytase on the absorption of P and divalent cations was studied. In the current experiment, phytase addition also increased fecal digestibility of the monovalent cations Na and K (6%, for both; P < 0.02). Na- and K-phytate complexes are highly soluble. For instance, Na-phytate is >96% soluble over the pH-range 0.3–11.2 (59). Therefore, it is likely that digestibility of these minerals is not inhibited by phytate; their absorption was not studied in vivo previously in this context.
Most of the extra-absorbed minerals were excreted in the urine, indicating that their availability was in excess of the piglets’ requirements. This corresponds with findings of O’Quinn et al. (19). In finishing swine, they recovered 79% of the extra-absorbed P in urine when phytase supplementation increased from 300 to 500 FTU/kg; at that level, the P requirement of swine was approached. In our experiment, using diets not limiting in P, the relative urinary loss of phytase-induced P absorption was 83%.
Effect of minerals on energy metabolism.
Absorption of many minerals is in part an active process that requires energy. Most minerals are excreted passively, but there is an extensive, partly active, reabsorption of minerals in the kidneys (60,61). Many active processes are driven by Na-K-ATPase. This enzyme generates a Na and K concentration gradient and electric potential difference, which drives the absorption of other ions and molecules (23,62). Na-K-ATPase–dependent respiration was estimated to be as high as 70% of kidney oxygen consumption (21,24). The work of the kidneys requires 14% of maintenance oxygen consumption (21,24); thus 10% of MEm would be related to mineral reabsorption in the kidney. Using our model, energy costs for mineral reabsorption from the kidney were estimated at 30 kJ/(kg0.75 · d) (mean of treatments; data not shown), or 7% of MEm. Our estimate seems low, indicating that the energy costs of urinary reabsorption may be underestimated.
When constructing the model, several assumptions were made, some of which potentially underestimate energy costs. These assumptions include: 1) Excretion of minerals by some organs, and possible subsequent reabsorption, is neglected. With saliva and other gastrointestinal juices, a large quantity of minerals is excreted into the gastrointestinal tract (63). Much of this is reabsorbed from the gut. The potential importance of mineral excretion in the gastrointestinal tract is illustrated by the relatively low ileal ash digestibility (64). 2) The potential energetic effect of the acid-base balance is not included in the calculations. This balance affects energy metabolism of piglets (65) and is probably altered by the extra amounts of minerals absorbed. On the other hand, some assumptions may lead to overestimation of the energy expenditure of mineral reabsorption. In particular, it is not always clear what proportion of the minerals is actively (re-) absorbed. We estimated these values on the basis of a number of references (60,66,67), but there are contrary views. For instance, the energy costs involved in the absorption of calcium from the gastrointestinal tract in humans are subject to debate (68–70).
Using the model, extra energy expenditure for membrane transport and for Ca and P deposition in bones was estimated at 4.6 kJ/(kg0.75 · d) for piglets administered phytase. This is equivalent to 1% of the estimated MEm. A sensitivity analysis of the model for energy costs of renal reabsorption of minerals showed especially the importance of measured urinary mineral excretion, which determines the calculated reabsorption coefficient of the minerals. For example, to equalize urinary sodium excretion to 3 mg/(kg0.75 · d), as measured in the experiment, a reabsorption coefficient of 0.964 was calculated. If this coefficient were fixed at 0.99, a value often mentioned in literature (60,66,67), calculated urinary excretion would be 1.1 mg/(kg0.75 · d). The higher reabsorption coefficient increases the estimated energy costs of renal sodium reabsorption by 39%.
Dietary treatment did not affect Htot, but the kinetics of heat production within the day showed some differences. For 3 of the hours from 7 through 12 h after afternoon feeding, Htot was higher in phytase-fed piglets (P < 0.05). Mean heat production during these 6 h was 8 (range 2–14) kJ/(kg0.75 · d) higher in phytase-fed than in control piglets. We speculate that this increased heat production was related to increased mineral excretion. A diurnal variation of mineral excretion was shown for P, Na, K, and Cl (71,72). The peak in urinary Na excretion shifted due to heat stress or work, in men in a hot environment (72). Diurnal shifts in mineral excretion could not be measured in the present experiment, nor could we measure whether a similar effect on heat production exists after morning feeding because it coincided with the heat production peak after the afternoon meal.
In conclusion, phytase addition improved nutrient digestibility. Because the extra energy digested was lost postabsorption, energy metabolizability was not affected. Furthermore, protein and fat deposition rates were unaffected by dietary phytase. Mineral absorption and subsequent urinary excretion were increased by phytase supplementation. Phytase-induced effects on organ weights and blood variables suggested that the energy expenditure of the digestive tract was reduced, and metabolic activity in visceral organs increased. The possible energy-saving benefits of supplemental phytase at the level of digestion might be counterbalanced by the increased energy costs for other processes, such as the increased absorption and urinary excretion of minerals. These costs were subsequently estimated, using a simulation model. Phytase-induced energy expenditure associated with increased (re-) absorption of protein, fatty acids, and minerals, and deposition of Ca and P in bone tissues was estimated to be just over 1% of MEm. The simultaneous existence of both increases and decreases in heat production processes resulted in the absence of a net effect on energy retention.
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FOOTNOTES |
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2 Appendix 1 is available with the online posting of this paper at www.nutrition.org.
4 Abbreviations used: DE, digestible energy; FTU, phytase unit (1 FTU is the amount of enzyme that liberates 1 µmol inorganic orthophosphate/min from a 5.1 mmol sodium phytate solution at pH 5.5 and 37°C); GE, gross energy; GLM, general linear model; Hact, heat production related to activity; Hrest, Heat production not related to activity (Htot –Hact); Htot, total heat production; ICP-AES, inductively coupled plasma atomic emission spectrometry; kRAM,pu,pl, rate of reabsorption of mineral M from primary urine to plasma; ME, metabolizable energy; MEm, metabolizable energy required for maintenance; pCO2, partial carbon dioxide pressure; pO2, partial oxygen pressure.
Manuscript received 13 August 2004. Initial review completed 22 September 2004. Revision accepted 31 January 2005.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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